Skip to main content Accessibility help

Dietary starch promotes hepatic lipogenesis in barramundi (Lates calcarifer)

  • N. M. Wade (a1), L. H. Trenkner (a1) (a2), I. Viegas (a3) (a4), L. C. Tavares (a3), M. Palma (a1), S. Skiba-Cassy (a5), K. Dias (a5), C. Vachot (a5), B. C. Araújo (a1) (a6), N. Bourne (a1), D. Blyth (a7), S. Irvin (a7) and B. D. Glencross (a1)...


Barramundi (Lates calcarifer) are a highly valued aquaculture species, and, as obligate carnivores, they have a demonstrated preference for dietary protein over lipid or starch to fuel energetic growth demands. In order to investigate how carnivorous fish regulate nutritional cues, we examined the metabolic effects of feeding two isoenergetic diets that contained different proportions of digestible protein or starch energy. Fish fed a high proportion of dietary starch energy had a higher proportion of liver SFA, but showed no change in plasma glucose levels, and few changes in the expression of genes regulating key hepatic metabolic pathways. Decreased activation of the mammalian target of rapamycin growth signalling cascade was consistent with decreased growth performance values. The fractional synthetic rate (lipogenesis), measured by TAG 2H-enrichment using 2H NMR, was significantly higher in barramundi fed with the starch diet compared with the protein diet (0·6 (se 0·1) v. 0·4 (se 0·1) % per d, respectively). Hepatic TAG-bound glycerol synthetic rates were much higher than other closely related fish such as sea bass, but were not significantly different (starch, 2·8 (se 0·3) v. protein, 3·4 (se 0·3) % per d), highlighting the role of glycerol as a metabolic intermediary and high TAG-FA cycling in barramundi. Overall, dietary starch significantly increased hepatic TAG through increased lipogenesis. Compared with other fish, barramundi possess a unique mechanism to metabolise dietary carbohydrates and this knowledge may define ways to improve performance of advanced formulated feeds.


Corresponding author

*Corresponding author: N. M. Wade, email


Hide All

Present address: Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, UK.



Hide All
1.Azevedo, PA, van Milgen, J, Leeson, S, et al. (2005) Comparing efficiency of metabolizable energy utilization by rainbow trout (Oncorhynchus mykiss) and Atlantic salmon (Salmo salar) using factorial and multivariate approaches. J Anim Sci 83, 842851.
2.Hua, K, Birkett, S, De Lange, CFM, et al. (2010) Adaptation of a non-ruminant nutrient-based growth model to rainbow trout (Oncorhynchus mykiss Walbaum). J Agric Sci 148, 1729.
3.Bureau, DP & Hua, K (2008) Models of nutrient utilization by fish and potential applications for fish culture operations. In Mathematical Modelling in Animal Nutrition, pp. 442461 [France, J and Kebreab, E, editors]. Wallingford: CAB International.
4.Dumas, A, France, J & Bureau, D (2010) Modelling growth and body composition in fish nutrition: where have we been and where are we going? Aquacult Res 41, 161181.
5.Saravanan, S, Schrama, JW, Figueiredo-Silva, AC, et al. (2012) Constraints on energy intake in fish: the link between diet composition, energy metabolism, and energy intake in rainbow trout. PLOS ONE 7, e34743.
6.Schrama, JW, Saravanan, S, Geurden, I, et al. (2012) Dietary nutrient composition affects digestible energy utilisation for growth: a study on Nile tilapia (Oreochromis niloticus) and a literature comparison across fish species. Br J Nutr 108, 277289.
7.Pérez-Jiménez, A, Carmen Hidalgo, M, Morales, AE, et al. (2009) Growth performance, feed utilization and body composition of Dentex dentex fed on different macronutrient combinations. Aquacult Res 41, 111119.
8.Pérez-Jiménez, A, Hidalgo, MC, Morales, AE, et al. (2009) Use of different combinations of macronutrients in diets for dentex (Dentex dentex): effects on intermediary metabolism. Comp Biochem Physiol Part A Mol Integr Physiol 152, 314321.
9.Glencross, B, Blyth, D, Irvin, S, et al. (2014) An analysis of the effects of different dietary macronutrient energy sources on the growth and energy partitioning by juvenile barramundi, Lates calcarifer, reveal a preference for protein-derived energy. Aquacult Nutr 20, 583594.
10.Polakof, S, Panserat, S, Soengas, JL, et al. (2012) Glucose metabolism in fish: a review. J Comp Physiol B 182, 10151045.
11.Moon, T (2001) Glucose intolerance in teleost fish: fact or fiction? Comp Biochem Phys B 129, 243249.
12.Viegas, I, Trenkner, LH, Rito, J, et al. (2019) Impact of dietary starch on extrahepatic tissue lipid metabolism in farmed European (Dicentrarchus labrax) and Asian seabass (Lates calcarifer). Comp Biochem Phys A 231, 170176.
13.Kamalam, BS, Medale, F & Panserat, S (2017) Utilisation of dietary carbohydrates in farmed fishes: new insights on influencing factors, biological limitations and future strategies. Aquaculture 467, 327.
14.Chen, YJ, Zhang, TY, Chen, HY, et al. (2017) An evaluation of hepatic glucose metabolism at the transcription level for the omnivorous GIFT tilapia, Oreochromis niloticus during postprandial nutritional status transition from anabolism to catabolism. Aquaculture 473, 375382.
15.Panserat, S, Rideau, N & Polakof, S (2014) Nutritional regulation of glucokinase: a cross-species story. Nutr Res Rev 27, 2147.
16.Froese, R & Pauly, D (editors) (2019) FishBase. World Wide Web electronic publication. (accessed December 2019).
17.Jerry, DR (2013) Biology and Culture of Asian Seabass, Lates calcarifer. Boca Raton, FL: CRC Press, Taylor and Francis Group.
18.Bermudes, M, Glencross, B, Austen, K, et al. (2010) The effects of temperature and size on the growth, energy budget and waste outputs of barramundi (Lates calcarifer). Aquaculture 306, 160166.
19.Glencross, B & Bermudes, M (2010) Effect of high water temperatures on the utilisation efficiencies of energy and protein by juvenile barramundi, Lates calcarifer. Fish Aquacult J 14, 111.
20.Glencross, BD (2008) A factorial growth and feed utilization model for barramundi, Lates calcarifer based on Australian production conditions. Aquacult Nutr 14, 360373.
21.Glencross, BD & Bermudes, M (2012) Adapting bioenergetic factorial modelling to understand the implications of heat stress on barramundi (Lates calcarifer) growth, feed utilisation and optimal protein and energy requirements – potential strategies for dealing with climate change? Aquacult Nutr 18, 411422.
22.Glencross, BD, Blyth, D, Bourne, N, et al. (2017) An analysis of partial efficiencies of energy utilisation of different macronutrients by barramundi (Lates calcarifer) shows that starch restricts protein utilisation in carnivorous fish. Br J Nutr 117, 500510.
23.Skiba-Cassy, S, Panserat, S, Larquier, M, et al. (2013) Apparent low ability of liver and muscle to adapt to variation of dietary carbohydrate:protein ratio in rainbow trout (Oncorhynchus mykiss). Br J Nutr 109, 13591372.
24.Wade, NM, Skiba-Cassy, S, Dias, K, et al. (2014) Postprandial molecular responses in the liver of the barramundi, Lates calcarifer. Fish Physiol Biochem 40, 427443.
25.Dai, W, Panserat, S, Mennigen, JA, et al. (2013) Post-prandial regulation of hepatic glucokinase and lipogenesis requires the activation of TORC1 signalling in rainbow trout (Oncorhynchus mykiss). J Exp Biol 216, 44834492.
26.Panserat, S & Kaushik, SJ (2010) Regulation of gene expression by nutritional factors in fish. Aquacult Res 41, 751762.
27.Lansard, M, Panserat, S, Seiliez, I, et al. (2009) Hepatic protein kinase B (Akt) – target of rapamycin (TOR)-signalling pathways and intermediary metabolism in rainbow trout (Oncorhynchus mykiss) are not significantly affected by feeding plant-based diets. Br J Nutr 102, 15641573.
28.Viegas, I, Mendes, VM, Leston, S, et al. (2011) Analysis of glucose metabolism in farmed European sea bass (Dicentrarchus labrax L.) using deuterated water. Comp Biochem Physiol A Mol Integr Physiol 160, 341347.
29.Viegas, I, Rito, J, Jarak, I, et al. (2015) Contribution of dietary starch to hepatic and systemic carbohydrate fluxes in European seabass (Dicentrarchus labrax L.). Br J Nutr 113, 13451354.
30.Viegas, II, Rito, JJ, Jarak, II, et al. (2012) Hepatic glycogen synthesis in farmed European seabass (Dicentrarchus labrax L.) is dominated by indirect pathway fluxes. Comp Biochem Physiol A Mol Integr Physiol 163, 2229.
31.Viegas, I, Jarak, I, Rito, J, et al. (2016) Effects of dietary carbohydrate on hepatic de novo lipogenesis in European seabass (Dicentrarchus labrax L.). J Lipid Res 57, 12641272.
32.Fisher, G, Arias, I, Quesada, I, et al. (2001) A fast and sensitive method for measuring picomole levels of total free amino acids in very small amounts of biological tissues. Amino Acids 20, 163173.
33.Coutteau, P & Sorgeloos, P (1995) Intercalibration Exercise on the Qualitative and Quantitative Analysis of Fatty Acids in Artemia and Marine Samples Used in Mariculture. Copenhagen: ICES.
34.Green, MR & Sambrook, J (2012) Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
35.Seiliez, I, Gabillard, JC, Skiba-Cassy, S, et al. (2008) An in vivo and in vitro assessment of TOR signaling cascade in rainbow trout (Oncorhynchus mykiss). Am J Physiol Regul Integr Comp Physiol 295, R329R335.
36.Matyash, V, Liebisch, G, Kurzchalia, TV, et al. (2008) Lipid extraction by methyl-tert-butyl ether for high-throughput lipidomics. J Lipid Res 49, 11371146.
37.Ruiz, J, Antequera, T, Andres, AI, et al. (2004) Improvement of a solid phase extraction method for analysis of lipid fractions in muscle foods. Anal Chim Acta 520, 201205.
38.Jones, JG, Merritt, M & Malloy, C (2001) Quantifying tracer levels of (H2O)-H-2 enrichment from microliter amounts of plasma and urine by H-2 NMR. Magn Reson Med 45, 156158.
39.Krebs, HA (1950) Chemical composition of blood plasma and serum. Annu Rev Biochem 19, 409430.
40.Viegas, I, Araujo, PM, Rocha, AD, et al. (2017) Metabolic plasticity for subcutaneous fat accumulation in a long-distance migratory bird traced by 2H2O. J Exp Biol 220, 10721078.
41.Duarte, JA, Carvalho, F, Pearson, M, et al. (2014) A high-fat diet suppresses de novo lipogenesis and desaturation but not elongation and triglyceride synthesis in mice. J Lipid Res 55, 25412553.
42.Enes, P, Panserat, S, Kaushik, S, et al. (2008) Nutritional regulation of hepatic glucose metabolism in fish. Fish Physiol Biochem 35, 519539.
43.Glencross, B, Blyth, D, Tabrett, S, et al. (2012) An assessment of cereal grains and other starch sources in diets for barramundi (Lates calcarifer) – implications for nutritional and functional qualities of extruded feeds. Aquacult Nutr 18, 388399.
44.Allan, GL, Booth, M, Stone, DAJ, et al. (2003) Aquaculture diet development subprogram: ingredient evaluation. N S W Fish Final Rep Ser 58, 150.
45.Panserat, S, Médale, F, Blin, C, et al. (2000) Hepatic glucokinase is induced by dietary carbohydrates in rainbow trout, gilthead seabream, and common carp. Am J Physiol Regul Integr Comp Physiol 278, 11641170.
46.Panserat, S, Plagnes-Juan, E & Kaushik, S (2002) Gluconeogenic enzyme gene expression is decreased by dietary carbohydrates in common carp (Cyprinus carpio) and gilthead seabream (Sparus aurata). Biochim Biophys Acta 1579, 3542.
47.Capilla, E, Médale, F, Navarro, I, et al. (2003) Muscle insulin binding and plasma levels in relation to liver glucokinase activity, glucose metabolism and dietary carbohydrates in rainbow trout. Regul Pept 110, 123132.
48.Enes, P, Panserat, S, Kaushik, S, et al. (2011) Dietary carbohydrate utilization by European sea bass (Dicentrarchus labrax L.) and gilthead sea bream (Sparus aurata L.) juveniles. Rev Fish Sci 19, 201215.
49.Meton, I, Caseras, A, Fernandez, F, et al. (2004) Molecular cloning of hepatic glucose-6-phosphatase catalytic subunit from gilthead sea bream (Sparus aurata): response of its mRNA levels and glucokinase expression to refeeding and diet composition. Comp Biochem Physiol B Biochem Mol Biol 138, 145153.
50.Caseras, A, Meton, I, Fernandez, F, et al. (2000) Glucokinase gene expression is nutritionally regulated in liver of gilthead sea bream (Sparus aurata). Biochim Biophys Acta 1493, 135141.
51.Skiba-Cassy, S, Polakof, S, Seiliez, I, et al. (2012) Functional genomic analysis of the nutritional and hormonal regulation of fish glucose and lipid metabolism. In Functional Genomics in Aquaculture, pp. 129146 [Saroglia, M and Liu, ZJ, editors]. Oxford: Wiley-Blackwell.
52.Caseras, A, Meton, I, Vives, C, et al. (2002) Nutritional regulation of glucose-6-phosphatase gene expression in liver of the gilthead sea bream (Sparus aurata). Br J Nutr 88, 607614.
53.Garcia-Rejon, L, Sanchez-Muros, MJ, Cerda, J, et al. (1997) Fructose 1,6 bisphosphatase activity in liver and gonads of sea bass (Dicentrarchus labrax). Influence of diet composition and stage of the reproductive cycle. Fish Physiol Biochem 16, 93105.
54.Bonamusa, L, De Frutos, PG, Fernandes, F, et al. (1992) Nutritional effects on key glycolytic-gluconeogenic enzyme activities and metabolite levels in the liver of the teleost fish Sparus Aurata. Mol Mar Biol Biotech 1, 113124.
55.Meton, I, Mediavilla, D, Caseras, A, et al. (1999) Effect of diet composition and ration size on key enzyme activities of glycolysis-gluconeogenesis, the pentose phosphate pathway and amino acid metabolism in liver of gilthead sea bream (Sparus aurata). Br J Nutr 82, 223232.
56.Enes, P, Panserat, S, Kaushik, S, et al. (2006) Effect of normal and waxy maize starch on growth, food utilization and hepatic glucose metabolism in European sea bass (Dicentrarchus labrax) juveniles. Comp Biochem Physiol A 143, 8996.
57.Kirchner, S, Kaushik, S & Panserat, S (2003) Low protein intake is associated with reduced hepatic gluconeogenic enzyme expression in rainbow trout (Oncorhynchus mykiss). J Nutr 133, 25612564.
58.Viegas, I, Rito, J, González, JD, et al. (2013) Effects of food-deprivation and refeeding on the regulation and sources of blood glucose appearance in European seabass (Dicentrarchus labrax L.). Comp Biochem Physiol A Mol Integr Physiol 166, 399405.
59.Polak, P & Hall, MN (2009) mTOR and the control of whole body metabolism. Curr Opin Cell Biol 21, 209218.
60.Borges, P, Valente, LMP, Veron, V, et al. (2014) High dietary lipid level is associated with persistent hyperglycaemia and downregulation of muscle Akt-mTOR pathway in senegalese sole (Solea senegalensis). PLOS ONE 9, e102196.
61.Ekmann, KS, Dalsgaard, J, Holm, J, et al. (2013) Effects of dietary energy density and digestible protein: energy ratio on de novo lipid synthesis from dietary protein in gilthead sea bream (Sparus aurata) quantified with stable isotopes. Br J Nutr 110, 17711781.
62.Ekmann, KS, Dalsgaard, J, Holm, J, et al. (2013) Glycogenesis and de novo lipid synthesis from dietary starch in juvenile gilthead sea bream (Sparus aurata) quantified with stable isotopes. Br J Nutr 109, 21352146.
63.Felip, O, Ibarz, A, Fernandez-Borras, J, et al. (2012) Tracing metabolic routes of dietary carbohydrate and protein in rainbow trout (Oncorhynchus mykiss) using stable isotopes ([13C]starch and [15N]protein): effects of gelatinisation of starches and sustained swimming. Br J Nutr 107, 834844.
64.Hemre, GI & Kahrs, F (1997) 14C-glucose injection in Atlantic cod, Gadus morhua, metabolic responses and excretion via the gill membrane. Aquacult Nutr 3, 38.
65.Hemre, GI & Storebakken, T (2000) Tissue and organ distribution of 14C-activity in dextrin-adapted Atlantic salmon after oral administration of radiolabelled 14C1-glucose. Aquacult Nutr 6, 229234.
66.Magnoni, L, Vaillancourt, E & Weber, JM (2008) High resting triacylglycerol turnover of rainbow trout exceeds the energy requirements of endurance swimming. Am J Physiol Regul Integr Comp Physiol 295, R309R315.
67.Gonzalez, JD, Caballero, A, Viegas, I, et al. (2012) Effects of alanine aminotransferase inhibition on the intermediary metabolism in Sparus aurata through dietary amino-oxyacetate supplementation. Br J Nutr 107, 17471756.
68.Gasier, HG, Previs, SF, Pohlenz, C, et al. (2009) A novel approach for assessing protein synthesis in channel catfish, Ictalurus punctatus. Comp Biochem Physiol B Biochem Mol Biol 154, 235238.
69.Castro, C, Corraze, G, Basto, A, et al. (2016) Dietary lipid and carbohydrate interactions: implications on lipid and glucose absorption, transport in gilthead sea bream (Sparus aurata) juveniles. Lipids 51, 743755.
70.Dai, WW, Panserat, S, Plagnes-Juan, E, et al. (2015) Amino acids attenuate insulin action on gluconeogenesis and promote fatty acid biosynthesis via mTORC1 signaling pathway in trout hepatocytes. Cell Physiol Biochem 36, 10841100.


Type Description Title
Supplementary materials

Wade et al. supplementary material
Wade et al. supplementary material 1

 Word (525 KB)
525 KB
Supplementary materials

Wade et al. supplementary material
Wade et al. supplementary material 2

 Word (29 KB)
29 KB

Dietary starch promotes hepatic lipogenesis in barramundi (Lates calcarifer)

  • N. M. Wade (a1), L. H. Trenkner (a1) (a2), I. Viegas (a3) (a4), L. C. Tavares (a3), M. Palma (a1), S. Skiba-Cassy (a5), K. Dias (a5), C. Vachot (a5), B. C. Araújo (a1) (a6), N. Bourne (a1), D. Blyth (a7), S. Irvin (a7) and B. D. Glencross (a1)...


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.